Hydrobiologia

https://doi.org/10.1007/s10750-020-04332-9 (0123456789().,-volV)
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89().,-volV)

COLIN S. REYNOLDS’ LEGACY Review Paper

Freshwater phytoplankton diversity: models, drivers

and implications for ecosystem properties
Gábor Borics . András Abonyi . Nico Salmaso . Robert Ptacnik

Received: 25 February 2020 / Revised: 9 June 2020 / Accepted: 13 June 2020

 The Author(s) 2020

Abstract Our understanding on phytoplankton diver-
sity has largely been progressing since the publication of
Hutchinson on the paradox of the plankton. In this paper,
we summarise some major steps in phytoplankton
ecology in the context of mechanisms underlying
phytoplankton diversity. Here, we provide a framework
for phytoplankton community assembly and an over-
view of measures on taxonomic and functional diversity.
We show how ecological theories on species competition
together with modelling approaches and laboratory
Guest editors: Judit Padisák, J. Alex Elliott, Martin T. Dokulil
& Luigi Naselli-Flores / New, old and evergreen frontiers in
freshwater phytoplankton ecology: the legacy of
Colin S. Reynolds
Electronic supplementary material The online version of
this article (https://doi.org/10.1007/s10750-020-04332-9) con-
tains supplementary material, which is available to authorized
users.
experiments helped understand species coexistence and
maintenance of diversity in phytoplankton. The non-
equilibrium nature of phytoplankton and the role of
disturbances in shaping diversity are also discussed.
Furthermore, we discuss the role of water body size,
productivity of habitats and temperature on phytoplank-
ton species richness, and how diversity may affect the
functioning of lake ecosystems. At last, we give an
insight into molecular tools that have emerged in the last
decades and argue how it has broadened our perspective
on microbial diversity. Besides historical backgrounds,
some critical comments have also been made.
Keywords Community assembly
Diversity
maintenance
Ecosystem functioning
Functional
diversity
Molecular approaches
Taxonomic
diversity

G. Borics (&) A. Abonyi
R. Ptacnik

Department of Tisza Research, Centre for Ecological WasserCluster Lunz – Biologische Station GmbH, Dr.
Research, Danube Research Institute, Bem tér 18/c, Carl Kupelwieser-Promenade 5, 3293 Lunz am See,
4026 Debrecen, Hungary Austria
e-mail: boricsg@gmail.com
N. Salmaso
G. Borics Research and Innovation Centre, Fondazione Edmund
GINOP Sustainable Ecosystems Group, Centre for Mach, Via E. Mach 1, 38010 San Michele all’Adige, Italy
Ecological Research, Klebelsberg Kuno u. 3,
8237 Tihany, Hungary

A. Abonyi
Centre for Ecological Research, Institute of Ecology and
Botany, Alkotmány u. 2-4, 2163 Vácrátót, Hungary

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Introduction
Phytoplankton is a polyphyletic group with utmost
variation in size, shape, colour, type of metabolism,
and life history traits. Due to the emerging knowledge
in nutritional capabilities of microorganisms, our view
of phytoplankton has drastically changed (Flynn et al.,
2013). Phagotrophy is now known from all clades
except diatoms and cyanobacteria. At the same time,
ciliates, which have not been considered as part of
‘phytoplankton’, span a gradient in trophic modes that
render the distinction between phototrophic phyto-
plankton and heterotrophic protozoa meaningless.
This complexity has been expressed in the high
diversity of natural phytoplankton assemblages.
Diversity can be defined in many different ways and
levels. Although the first diversity measure that
encompassed the two basic components of diversity
(i.e., the number of items and their relative frequen-
cies) appeared in the early forties of the last century
(Fisher et al., 1943), in phytoplankton ecology,
taxonomic richness has been used the most often as
diversity estimates. Until the widespread use of the
inverted microscopes, phytoplankton ecologists did
not have accurate abundance estimation methods and
the net plankton served as a basis for the analyses.
Richness of taxonomic groups of net samples, and
their ratios were used for quality assessment (Thun-
mark, 1945, Nygaard, 1949).
The study of phytoplankton diversity received a
great impetus after Hutchinson’s (1961) seminal paper
on the paradox of the plankton. The author not only
contrasted Hardin’s competitive exclusion theory
(Hardin, 1960) with the high number of co-occurring
species in a seemingly homogeneous environment, but
outlined possible explanations. He argued for the non-
equilibrium nature of the plankton, the roles of
disturbances and biotic interactions, moreover the
importance of benthic habitats in the recruitment of
phytoplankton. The ‘paradox of the plankton’ largely
influenced the study of diversity in particular and the
development of community ecology in general
(Naselli-Flores & Rossetti, 2010). Several equilibrium
and non-equilibrium mechanisms have been devel-
oped to address the question of species coexistence in
pelagic waters (reviewed by Roy & Chattopadhyay,
2007). The paradox and the models that aimed to
explain the species coexistence in the aquatic envi-
ronment have been extended to terrestrial ecosystems
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(Wilson, 1990). Wilson reviewed evidences for twelve
possible mechanisms that potentially could explain the
paradox for indigenous New Zealand vegetation, and
found that four of them, such as gradual climate
change, cyclic successional processes, spatial mass
effect and niche diversification, were the most impor-
tant explanations. By now, the paradox has been
considered as an apparent violation of the competitive
exclusion principle in the entire field of ecology
(Hening & Nguyen, 2020).
Although Hutchinson’s contribution (Hutchinson,
1961) has given a great impetus to research on species
coexistence, the number of studies on phytoplankton
diversity that time did not increase considerably
(Fig. 1), partly because in this period, eutrophication
studies dominated the hydrobiological literature.
Understanding the drivers of diversity has been
substantially improved from the 70 s when laboratory
experiments and mathematical modelling proved that
competition theory or intermediate disturbance
hypothesis (IDH) provided explanations for species
coexistence. Many field studies also demonstrated the
role of disturbances in maintaining phytoplankton
diversity, and these results were concluded by
Reynolds and his co-workers (Reynolds et al., 1993).
From the 2000 s a rapid increase in phytoplankton
research appeared (Fig. 1), which might be explained
by theoretical and methodological improvements in
ecology. The functional approaches—partly due to
Colin Reynolds’s prominent contribution to this field
(Reynolds et al., 2002)—opened new perspectives in
phytoplankton diversity research. Functional trait and
functional ‘group’-based approaches have gained
considerable popularity in recent years (Weithoff,
800
700
600
500
400
300
200
100
0
1960 1970 1980 1990 2000 2010 2020
Fig. 1 Annual number of hits on Google Scholar for the
keywords ‘‘phytoplankton diversity’’
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2003; Litchman & Klausmeier, 2008; Borics et al.,
2012; Vallina, et al., 2017; Ye et al., 2019).
Analysis of large databases enabled to study
diversity changes on larger scales in lake area,
productivity or temperature (Stomp et al., 2011).
Recent studies on phytoplankton also revealed that
phytoplankton diversity was more than a single metric
by which species or functional richness could be
described, instead, it was an essential characteristic,
which affects functioning of the ecosystems, such as
resilience (Gunderson 2000) or resource use efficiency
(Ptacnik et al., 2008; Abonyi et al., 2018a, b).
The widespread use of molecular tools that reor-
ganise phytoplankton taxonomy and reveal the pres-
ence of cryptic diversity, has changed our view of
phytoplankton diversity. In this study, we aim to give
an overview of the above-mentioned advancements in
phytoplankton diversity. Here we focus on the
following issues:
• measures of diversity,
• mechanisms affecting diversity,
• changes of diversity along environmental gradients
(area, productivity, temperature),
• the functional diversity–ecosystem functioning
relationship, and
• phytoplankton diversity using molecular tools.
More than eight thousand studies have been pub-
lished on ‘‘phytoplankton diversity’’ since the term
first appeared in the literature in the middle of the last
century (Fig. 1), therefore, in this review we cannot
completely cover all the important developments
made in recent years. Instead, we focus on the most
relevant studies considered as milestones in the field,
and on the latest relevant contributions. This study is a
part of a Hydrobiologia special issue dedicated to the
memory of Colin S. Reynolds, who was one of the
most prominent and influential figures of phytoplank-
ton ecology in the last four decades, therefore, we have
placed larger emphasis on his concepts that helped our
understanding of assembly and diversity of
phytoplankton.
Measures of diversity
In biology, the term ‘‘diversity’’ encompasses two
basic compositional properties of assemblages: spe-
cies richness and inequalities in species abundances.
Verbal definitions of diversity cannot be specific
enough to describe both aspects, but these can be
clearly defined by the mathematical formulas that we
use as diversity measures.
Richness metrics
The simplest measure of diversity is species richness,
that is, the number of species observed per sampling
unit. However, this metric can only be used safely
when the applied counting approach ensures high
species detectability.
In case of phytoplankton, species detectability
depends strongly on counting effort, therefore, mea-
sures that are standardised by the number of individ-
uals observed, e.g. Margalef and Mehinick indices
(Clifford & Stephenson, 1975) safeguard against
biased interpretations. Ideally, standardization should
take place in the process of identification. Pomati et al.
(2015) gave an example how a general detection limits
could be applied in retrospect to data stemming from
variable counting efforts.
Species richness can also be given using richness
estimators. These can be parametric curve-fitting
approaches, non-parametric estimators, and extrapo-
lation techniques using species accumulation or
species-area curves (Gotelli & Colwell, 2011; Magur-
ran, 2004). These approaches have been increasingly
applied in phytoplankton ecology (Naselli-Flores
et al., 2016; Görgényi et al., 2019).
Abundance-based metrics
Classical diversity metrics such as Shannon and
Simpson indices combine richness and evenness into
univariate vectors. Though used commonly in the
literature, they are prone to misinform about the actual
changes in a community, as they may reflect changes
in evenness and/or richness to an unknown extent (a
change in Shannon H’ 1948) may solely be driven by a
change in evenness or richness). Dominance metrics
emphasise the role of the most important species
(McNaughton, 1967). Rarity metrics, in contrast,
focus on the rare elements of the assemblages (Gotelli
& Colwell, 2011).
Species abundance distributions (SAD) and rank
abundance distributions (RAD: ranking the species’
abundances from the most abundant to the least
abundant) provide an alternative to diversity indices
(Fisher et al., 1943; Magurran & Henderson, 2003).
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These parametric approaches give accurate informa-
tion on community structure and are especially useful
when site level data are compared. Most RADs follow
lognormal distributions and allow to estimate species
richness in samples (Ulrich & Ollik, 2005).
Mechanisms affecting diversity
Community assembly
Understanding the processes that shape the commu-
nity structure of phytoplankton requires some knowl-
edge on the general rules of community assembly.
Models and mechanisms, which have been proposed
to explain the compositional patterns of biotic com-
munities, can be linked together under one conceptual
framework developed by Vellend (2010, 2016). Vel-
lend proposed four distinct processes that determine
species composition and diversity: speciation (cre-
ation of new species, or within-species genetic mod-
ifications), selection (environmental filtering, and
biotic interactions), drift (demographic stochasticity)
and dispersal (movement of individuals). The four
processes interact to determine community dynamics
across spatial scales from global, through regional to
local. The importance of the processes strongly
depends on the type of community, and the studied
spatial and temporal scales (Reynolds, 1993).
Importance of evolutionary processes in the com-
munity assembly have been demonstrated by several
phylogenetic ecological studies (Cavender-Bares
et al., 2009) and also indicated by the emergence of
a new field of science called ecophylogenetics (Mou-
quet et al., 2012). As far as the phytoplankton is
concerned, the role of speciation can be important
when the composition and diversity of algal assem-
blages are studied at large (global) spatial scales.
However, we may note that although microscopic
analyses cannot grasp it, short-term evolutionary
processes do occur locally in planktic assemblages
(Balzano et al., 2011; Padfield et al., 2016; Bach et al.,
2018).
Demographic stochasticity influences growth and
extinction risk of small populations largely (Parvinen
et al., 2003; Méndez et al., 2019). Similarly, it might
also act on large lake phytoplankton since population
size in previous years affects the success of species in
the subsequent year. Small changes in initial abun-
dances may have strong effects on seasonal
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development. Demographic stochasticity, however,
is crucial in small isolated waters (especially in newly
created ones) where the sequence of new arrivals and
small differences in initial abundances likely have a
strong effect on the outcome of community assembly.
Theoretical models, laboratory experiments and
field studies demonstrated that the other two pro-
cesses, selection and dispersal, have a pivotal role in
shaping community assembly and diversity. Although
this statement corresponds well with the Baas-Becking
(1934) hypothesis (everything can be everywhere but
environment selects), importance of selection and
dispersal depends on the characteristics of the aquatic
systems. Selection and dispersal can be considered as
filters (Knopf, 1986, Pearson et al., 2018), and using
them as gradients, a two-dimensional plane can be
constructed, where the positions of the relevant types
of pelagic aquatic habitats can be displayed (Fig. 2).
At high dispersal rate, the mass effect (or so-called
source-sink dynamics) is the most decisive process
affecting community assembly (Leibold & Chase,
2017). Phytoplankton of rhithral rivers is a typical
example of the sink populations because its compo-
sition and diversity are strongly affected by the
propagule pressure coming partly from the source
populations of the benthic zone and from the limnetic
habitats of the watershed (Bolgovics et al., 2017). The
relative importance of the mass effect decreases with
time and with the increasing size of the river, while the
role of selection (species sorting) increases. Due to
their larger size, the impact of the source-sink
dynamics in potamal rivers must be smaller, and
selection becomes more important in shaping
Fig. 2 Positions of the relevant types of pelagial aquatic
habitats in the selection/dispersal plane
Hydrobiologia
community assembly. Although the role of spatial
processes in lake phytoplankton assembly cannot be
ignored, their importance is considerably less than that
of the locally acting selection. Relevance of the spatial
processes have been demonstrated for river floodplain
complexes (Vanormelingen et al., 2008; Devercelli
et al., 2016; Bortolini et al., 2017), or for the lakes of
Fennoscandia (Ptacnik et al., 2010a, b), where the
large lake density facilitates the manifestation of
spatially acting processes. High selection and low
dispersal represent the position of phytoplankton
inhabiting isolated lakes. Reviewing the literature of
algal dispersal Reynolds concluded (2006) that cos-
mopolitan and pandemic distribution of algae is due to
the fact that most of the planktic species effectively
exploit the dispersal channels. However, he also noted
that several species are not good dispersers, therefore,
endemism might occur among algae.
Composition and diversity of these assemblages are
controlled by the locally acting environmental filtering
and by biotic interactions, frequently, by competition.
The environmental filtering metaphor appears in
Reynolds’ habitat template approach (Reynolds,
1998), where the template is scaled against quantified
gradients of energy and resource availability. The
template represents the filter, while the habitats mean
the porosity (Reynolds, 2003). Species that manage to
pass the filter are the candidate components of the
assemblages. Finally, low-level biotic interactions
(Vellend, 2016) determine the composition and
diversity of the communities.
The four mechanisms, proposed by Vellend, act
differently on the various metric values of diversity.
Using the special cases of Rényi’s entropy (a: ? 0, 1,
2, ?) (ESM Box 1) we can show how mechanisms
influence species richness and species inequalities,
and how they act on the metrics between these
extremes (ESM Table 1). Drivers of functional diver-
sity are identical with that of species diversity, but
their impacts are attenuated by the functional redun-
dancy of the assemblages.
The role of competition in the maintenance of diversity
The concept of competition and coexistence has been
first proved experimentally both for artificial two-
species systems (Tilman & Kilham, 1976; Tilman,
1977) and for natural phytoplankton assemblages
(Sommer, 1983). However, limitations by different
nutrients are responsible only for a small portion of
diversity, even if the micronutrients are also included.
Therefore, it was an important step when Sommer
(1984) applying a pulsed input of one key nutrient in a
flow-through culture managed to maintain the coex-
istence of several species; although they were com-
peting for the same resource. Several competition
experiments have been carried out in recent years
demonstrating the role of inter- (Ji et al., 2017) and
intra-specific competition (Sildever et al., 2016) in the
coexistence of planktic algae.
The fact that one single resource added in pulses
can maintain the coexistence of multiple species has
been also proved by mathematical modelling (Eben-
höh, 1988). Using deterministic models, Huisman &
Weissing (1999) showed that competition for three or
more resources result in sustained species oscillations
or chaotic dynamics even under constant resource
supply. These oscillations in species abundance make
possible the coexistence of several species on a few
limiting resources (Wang et al., 2019).
The non-equilibrium nature of phytoplankton
and the role of disturbances
One of the underlying assumptions of the classical
competition theories is that species coexistence
requires a stable equilibrium point (Chesson & Case,
1986). However, the stable equilibrium state is not a
fundamental property of ecosystems (DeAngelis &
Waterhouse, 1987; Hastings et al., 2018). Hutchinson
put forward the idea that phytoplankton diversity
could be explained by ‘‘permanent failure to achieve
equilibrium’’ (Hutchinson, 1941). On a sufficiently
large timescale, ecosystems seem to show transient
dynamics, and do not necessarily converge to an
equilibrium state (Hastings et al., 2018). However, the
virtually static equilibrium-centred view of ecological
processes cannot explain the transient behaviour of
ecosystems (Holling, 1973; Morozov et al., 2019).
Today, there is a broad consensus in phytoplankton
ecology that composition and diversity of phytoplank-
ton can be best explicable by non-equilibrium
approaches (Naselli-Flores et al., 2003). The non-
equilibrium theories do not reject the role of compe-
tition in community assembly but place a larger
emphasis on historical effects, chance factors, spatial
inequalities, environmental perturbations (Chesson &
Case, 1986), and transient dynamics of the ecosystems
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(Hastings, 2004). The interactions among the inter-
nally driven processes and the externally imposed
stochasticity of environmental variability as an expla-
nation of community assembly have been conceptu-
alized in the Intermediate Disturbance Hypothesis
(IDH) (Connell, 1978). This hypothesis predicts a
unimodal relationship between the intensities and
frequencies of disturbances and species richness.
Although this hypothesis has been developed for
macroscopic sessile communities, it has become
widely accepted in phytoplankton ecology (Sommer,
1999). It has been proposed that the frequency of
disturbances has to be measured on the scale of
generation times of organisms (Reynolds, 1993;
Padisák, 1994). Field observation suggested that
diversity peaked at disturbance frequency of 3–5
generation times (Padisák et al., 1988), which was also
corroborated by laboratory experiments (Gaedeke &
Sommer, 1986; Flöder & Sommer, 1999). The IDH,
however, is not without weaknesses (Fox, 2013).
Recognition and measurement of disturbance are
among the main concerns (Sommer et al., 1993).
Diversity changes are measured purely as responses to
unmeasured events (disturbances) (Juhasz-Nagy,
1993), which readily leads to circular reasoning.
Repeated disturbances might change the resilience of
the system, which modifies the response of commu-
nities and makes the impact of disturbances on
diversity unpredictable (Hughes, 2012).
Amalgamation of the equilibrium and non-equilibrium
concepts
The existence of the equilibrium and non-equilibrium
explanations of species coexistence represents a real
dilemma in ecology. Being sufficiently different, and
thus avoid strong competition, or sufficiently similar
with ecologically irrelevant exclusion rates (as it is
suggested by Hubbell’s neutral theory (2006)) are both
feasible strategies for species (Scheffer & van Nes,
2006). Coexistence of species with these different
strategies is also feasible if the many sufficiently
similar species create clusters along the niche axes (in
accordance with Hubbel’s (2006) neutral theory), and
the competitive abilities within the clusters are
sufficiently large. It has been demonstrated that the
so-called ‘‘lumpy coexistence’’ is characteristic for
phytoplankton assemblages (Graco-Roza et al., 2019).
Lumpy coexistence arises in fluctuating resource
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environments (Sakavara et al., 2018; Roelke et al.,
2019), and show higher resilience to species invasions
(Roelke & Eldridge, 2008) and higher resistance to
allelopathy (Muhl et al., 2018).
The model of lumpy coexistence has its roots in
mechanistic modelling of species coexistence (Schef-
fer & van Nes, 2006). Analysing lake phytoplankton
data Reynolds (1980, 1984, 1988) demonstrated that
species with similar preferences and tolerances to
environmental constraints like nutrients or changes in
water column stratification frequently coexist. These
empirical observations were formalised later in the
functional group (FG) concept (Reynolds et al., 2002).
Despite their different theoretical backgrounds, the
two approaches came to identical conclusions: species
having similar positions on the niche axes form
species clusters (or FGs), and in natural assemblages
clusters or FGs coexist. Thus, the concept of lumpy
coexistence can also be considered as a mechanistic
explanation of the Reynolds’s FG concept.
The mechanisms and forces detailed above can
explain how diversity is maintained at the local scale.
Recent metacommunity studies, however, indicate
that spatial processes have a crucial role in shaping
phytoplankton diversity (Devercelli et al., 2016;
Bortolini et al., 2017; Guelzow et al., 2017; Benito
et al., 2018). Despite the increasing research activity in
this field, spatial processes are far less studied than
local ones. More in-depth knowledge on the role of
connectivity of aquatic habitats and dispersal mech-
anisms of the phytoplankters will contribute to better
understand phytoplankton diversity at regional or
global scales.
Changes of diversity along environmental scales
Species–area relationships across systems
The area dependence of species richness deserved
special attention in ecology both from theoretical and
practical points of view. The increase of species
number with the area sampled is an empirical fact
(Brown & Lomolino, 1998). The first model that
described the so-called species–area relationship
(SAR) appeared first by Arrhenius (1921) who
proposed to apply power law for predicting species
richness from the surveyed area. Because of the
differences in the studied size scale and the studied
organism groups, several other models have also been
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proposed such as the exponential (Gleason, 1922), the
logistic (Archibald, 1949) and the linear (Connor &
McCoy, 1979) models. However, the power-law
(S = c 9 Az, where S: number of species; A: area
sampled; c: the intercept, z: the exponent) is still the
most widely used formula in SAR studies. The rate of
change of the slope with an increasing area (z value)
depends on the studied organisms, and also on the
localities. High values (z: 0.1–0.5) were reported for
macroscopic organisms (Durrett & Levin, 1996),
while low z values characterised (z: 0.02–0.08) the
microbial systems (Azovsky, 2002; Green et al. 2004;
Horner-Devine et al. 2004).
The phytoplankton SAR appeared first in Hutchin-
son’s (1961) paper, where he analysed Ruttner’s
dataset on Indonesian (Ruttner, 1952), and Järnefelt’s
(1956) data on Finnish lakes. He concluded that there
was no significant relationship between the area and
species richness. Hutchinson reckoned that contribu-
tion of the littoral algae to the phytoplankton might be
relevant, and because the littoral/pelagic ratio
decreases with lake size, this contribution also
decreases. Therefore, species richness cannot increase
with lake area. In a laboratory experiment, Dickerson
& Robinson (1985) found that large microcosms had
significantly smaller species richness values than
small ones. Based on laboratory studies, published
species counts from ponds lakes and oceans, Smith
et al. (2005) studied phytoplankton SAR in the
possible largest size scale (10-9 to 107 km2). They
demonstrated a significant positive relationship
between area and species richness. The calculated
z value (z = 0.134) was higher than those reported in
other microbial SAR studies. However, we note that
this study suffers from a methodological shortcoming,
because of differences in compilation of species
inventories. Therefore, the results are only suggestive
of possible trends that should be investigated more
thoroughly.
Analysing phytoplankton monitoring data of 540
lakes in the USA Stomp et al. (2011) found only a
slight increase in richness values with a considerable
amount of scatter in the data. The covered size range
was small in this study, and the applied counting
techniques could lead to bias in richness estimation.
Phytoplankton species richness showed a similar weak
relationship with lake size for Scandinavian lakes
(Ptacnik et al., 2010a, b), although the counting effort
was much better standardised. All the above studies
suggested that species richness was not independent of
water body size. However, because of the method-
ological differences, and differences in the covered
water body size, in richness estimation or the type of
the water bodies, any conclusions based on these
results should be handled with caution.
Nutrients, latitudinal and altitudinal differences
(Stomp et al., 2011) or the size of the regional species
pool (Fox et al., 2000, Ptacnik et al., 2010a, b) also
influence phytoplankton diversity. To reduce the
impact of these factors, Várbı́ró et al. (2017)
investigated phytoplankton SAR in a series of
standing waters within the same ecoregion and with
similar nutrient status. The water bodies covered ten
orders of magnitude size range (10-2 to 108 m2). In
this study, both the sampling effort and the sample
preparation was standardised. The authors demon-
strated that species richness did not scale mono-
tonously with water body size. They managed to show
the presence of the so-called Small Island Effect (SIE,
Lomolino & Weiser, 2001), the phenomenon, when
below a certain threshold area (here 10-2 to 102 m2
size range) species richness varies independently of
island size. A right-skewed hump-shaped relationship
was found between the area and phytoplankton species
richness with a peak at 105–106 m2 area. This
phenomenon has been called as Large Lake Effect
(LLE) by the authors, and they explained it by the
strong wind-induced mixing, which acts against
habitat diversity in the pelagic zones of large lakes.
The significance of this study is that its results help
explain the controversial results of earlier phytoplank-
ton SAR studies. The LLE explains why the species
richness had not grown in the case of the Ruttner’s and
Jarnefelt’s dataset. The SIE, however, explains why
Dickerson & Robinson (1985) found opposite tenden-
cies to SAR in microcosm experiments. Detailed
analysis of the phytoplankton in those water bodies
that produced the peak in the SAR curve in the study of
Várbı́ró et al. (2017) demonstrated that high diversity
has been caused by the intrusion of metaphytic
elements to the pelagic zone (Görgényi et al., 2019),
which can be considered as a within-lake metacom-
munity process.
Productivity–diversity relationships
Despite the more than half a century-long history of
investigations on the productivity/diversity
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relationship (PDR), the shape of the relationship and
the underlying mechanisms still remain a subject of
debate. The models describing the PDR vary from the
monotonic increasing, through the hump shaped and
u-shaped to the monotonic decreasing types in the
literature (Waide et al., 1999). In the PDR studies,
there are great differences in the applied scale (local/
regional/global), in the metric used to define produc-
tivity (e.g., nutrients, biomass, production rate, pre-
cipitation, evaporation), in the used diversity metrics,
and also in the studied group of organisms (special
phylogenetic groups, functional assemblages) (Mit-
telbach et al., 2001). PDR studies also have other
methodological and statistical problems (Mittelbach
et al., 2001). These differences in approaches may
generate different patterns, which lead to confusion
and inconclusive results (Whittaker & Heegaard,
2003; Hillebrand & Cardinale, 2010). Despite these
uncertainties, the most general PDR patterns are the
hump-shaped and positive linear relationships; the first
has been observed mostly in the case of local, while
the second in the case of regional scale studies (Chase
& Leibold, 2002; Ptacnik et al., 2010a). These patterns
are so robust that they have been shown for various
organisms independently from the highly different
proxies applied to substitute the real productivity.
The number of studies that explicitly focus on
phytoplankton PDR is few. The view that phytoplank-
ton diversity peaks at intermediate productivity level
has been demonstrated by several authors (Ogawa &
Ichimura, 1984; Agustı́ et al., 1991; Leibold, 1999).
This is greatly due to the fact that phytoplankton
studies fortunately do not suffer from scaling problem:
most studies use sample-based local a–s as diversity
metrics and nutrients or biomass (Chl-a) as a surrogate
measure of productivity. Unimodal relationships were
found for Czech (Skácelová & Lepš, 2014) and
Hungarian water bodies (Borics et al., 2014). Diversity
peaked in both cases at the 101–102 mg L-1 biovol-
ume range, characteristic for eutrophic lakes.
It has also been demonstrated that the unimodal
relationship was also true for the functional richness/
productivity relationship (Borics et al., 2014; Török
et al., 2016). Differences were also found between the
species richness and functional richness peaks; the
latter peaked at smaller biovolume range (Török et al.,
2016). We note here that all three studies were based
on monitoring data, and because of the applied sample
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processing, species richness values might be slightly
underestimated.
Several theories have been proposed to explain this
unimodal pattern. Moss (1973) reckoned that the
relationship could be accounted for by that the
populations of oligotrophic and eutrophic lakes over-
lapping at the intermediate productivity range. Rosen-
zweig’s (1971) paradox of enrichment hypothesis
explained the unimodal relationship by the destabi-
lized predator–prey relationship at enhanced produc-
tivity level. Tilman’s resource heterogeneity model
(1985) predicts that the coexistence of competing
species is enhanced when the supply of alternative
resources is heterogeneous both spatially and tempo-
rally. This heterogeneity increases with resource
supply together with species richness up to the point
when richness declines because the correlation
between spatiotemporal heterogeneity and resource
supply disappeares. The resource-ratio hypothesis can
also provide an explanation of the hump shaped PDR
(Tilman & Pacala, 1993; Leibold, 1997). This theory
suggests that relative supply of resources generates
variations in species composition. Identity of the most
strongly limiting resource changes, and at very high
resource supply (on the descending end of the curve)
only a few K-strategist specialists will prevail. The
species pools overlap at intermediate productivity
level, resulting in high species richness. This expla-
nation seems to be reasonable for phytoplankton PDR
studies.
Investigating the PDR in fishless ponds, Leibold
(1999) found that his results could be best explained
by the keystone predation hypothesis (Paine, 1966).
This theory asserts that at low productivity exploita-
tive competition is the main assembly rule, while with
increasing productivity range the role of predator
avoidance becomes more important.
The number of various explanations illustrates the
complexity of processes affecting the shape of the
PDR. The shifting effects of bottom-up vs. top-down
control on the trophic gradient, the size of the regional
species pool, that is, the number of potential coloniz-
ers, or the history of the studied water bodies
(naturally eutrophic lakes are studied, or eutrophicated
formerly oligotrophic ones) can considerably modify
the properties of the PDRs.
With a few exceptions (Irigoien et al., 2004),
phytoplankton PDRs have been studied almost exclu-
sively in standing waters.
Hydrobiologia
Investigating the phytoplankton PDRs in rivers
Borics et al. (2014) found monotonic increasing
pattern in rhithral and monotonic decreasing PDR in
potamal rivers. They explained the positive linear
PDR with the newly arriving species from the various
adjacent habitats of the watershed, which resulted in
high phytoplankton diversity even at highly eutrophic
conditions. This phytoplankton is a mixture of those
elements that enter the river from the connected water
bodies of various types. In contrast, potamal rivers are
highly selective environments in which the phyto-
plankton succession frequently terminates in low
diversity plankton dominated by K strategist centric
diatoms (Cyclotella and Stephanodiscus spp.).
We note here that study of the regional phyto-
plankton PDR should be an important and challenging
area of future work, which is presently hindered by the
disconnected databases and by difficulties in measur-
ing regional productivity.
Linkage between diversity and the metabolic theory
of ecology
Metabolism controls patterns, processes and dynamics
at each level of biological organisation from single
cells to ecosystems, summarised as the metabolic
theory of ecology (Brown et al., 2004). Metabolic
theory (MTE) provides alternative explanations for
observations on various fields of ecology such as in
individual performance, life history, population and
community dynamics, as well as in ecosystem pro-
cesses. According to MTE, dynamics of metabolic
processes have implications for species diversity.
Metabolic processes influence population growth and
interspecific competition, might accelerate evolution-
ary dynamics and the rate of speciation (Brown et al.,
2004). The direct linkage between temperature and
metabolic rate raises the possibility of new explana-
tions of the well-known latitudinal dependence of
species richness. Allen et al. (2002) found that for both
terrestrial and aquatic environments natural logarithm
of species richness should be a linear function of the
mean temperature of the environment. This model has
been tested both for lake and oceanic phytoplankton.
Investigating more than 600 European, North and
South American lakes Segura et al. (2015) found a
pronounced effect of temperature on species diversity
between 11 and 17 C. Righetti et al. (2019) analysed
the results of more than 500,000 phytoplankton
observations from the global ocean, and also showed
the relationship between temperature and species
richness, but similarly to freshwater lakes the rela-
tionship was not monotonic for the whole temperature
gradient. These results suggest that the MTE can be a
possible explanation for the temperature dependence
of diversity. However, we note that other theories
emphasising longer ‘‘effective’’ evolutionary time
(Rohde, 1992) or higher resource availability (Brown
& Lomolino, 1998) can also explain this general
pattern.
The functional diversity–ecosystem functioning
relationship in phytoplankton
More diverse communities perform better in terms of
resource use and ecosystem stability (Naeem & Li,
1997); known as the biodiversity-ecosystem function-
ing relationship (BEF). Similar to BEF relationships
shown in terrestrial plant communities (Tilman et al.,
1996, 1997), positive BEF relationships have also
been evidenced in both natural and synthetic phyto-
plankton communities (Ptacnik et al., 2008; Striebel
et al., 2009; Stockenreiter et al., 2013). The BEF
relationship itself, however, does not explain the
mechanisms underlying the relationship. The most
often recognised mechanisms are complementarity
(Loreau & Hector, 2001) and sampling effect (Fridley,
2001). Complementarity means that more diverse
communities complement each other in resource use
in a more efficient way. Sampling effect, on the other
hand, means that the chance increases for the presence
of species with effective functional attributes in more
diverse communities (Naeem & Wright, 2003).
In an attempt to get mechanistic understanding of
diversity-functioning relationships, there is a growing
interest in quantifying functional diversity of ecolog-
ical communities (Hillebrand & Matthiessen, 2009).
Functional diversity summarizes the values and ranges
of traits that influence ecosystem functioning (Petchey
& Gaston, 2006). By translating taxonomic into
functional diversity, we may eventually also distin-
guish complementarity from sampling effect.
In phytoplankton ecology, two functional perspec-
tives have been developing. First, the identification of
morphological, physiological and behavioural traits
(Weithoff, 2003; Litchman & Klausmeier, 2008) that
affect fitness (Violle et al., 2007) and are, therefore,
functional traits. Traits have been used in
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phytoplankton ecology at least since Margalef’s ‘life
forms’ concept (Margalef, 1968; 1978), even if they
were not referred to ‘traits’ explicitely (Weithoff &
Beisner, 2019). Second, the recognition of character-
istic functional units within phytoplankton assem-
blages led to the development of functional group
(ecological groups) concepts (see Salmaso et al.,
2015). These are the phytoplankton functional group
concept sensu Reynolds (FG, Reynolds et al., 2002),
the morpho-functional group concept (MFG, Salmaso
& Padisák, 2007), and the morphological group
concept (MBFG, Kruk et al., 2011).
The functional trait concept has been advocated in
trait-based models (Litchman et al., 2007) and aimed
at translating biotic into functional diversity, which
eventually would allow quantify functional diversity
at the community level. The functional trait concept
has recently been reviewed in context of measures and
approaches in marine and freshwater phytoplankton
(Weithoff & Beisner, 2019). On the other hand, the
‘functional group’ concepts have rather been devel-
oped in the context of describing characteristic
functional community compositions in specific set of
environment conditions (that is, the functional com-
munity–environment relationship).
The simplest functional diversity measure of phy-
toplankton is the number of ‘functional units’ in
assemblages. That is, either the number of unique
combinations of functional traits or the number of
ecological groups indentified. One way to use func-
tional units is to convert them into univariate measures
corresponding to those calculated from taxonomic
information (e.g., richness, evenness). Or, trait data
also allow the calculation of community-level means
of trait values (CWM) as an index of functional
community composition (Lavorel et al., 2008).
Second, one may consider calculate the components
of functional diversity (FD) such as functional rich-
ness, functional evenness, and functional divergence
(Mason et al., 2005); all representing independent
factes of functional community compositions. The
same FD concept has been developed further account-
ing also for the abundance of taxa within a multidi-
mensional trait space based on functional evenness,
functional divergence and functional dispersion (Lal-
iberté & Legendre, 2010). The recently developed
‘FD’ R package enables one to calculated easily all the
aforementioned FD measures (Laliberté & Legendre,
2010; Laliberté et al., 2014). The use of FD
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components in the context of BEF in phytoplankton
has only started very recently (Abonyi et al., 2018a, b;
Ye et al., 2019). Trait-based functional diversity
measures in BEF have recently been reviewed by
Venail (2017).
The functional community composition–environment
relationship
Functional traits can be classified as those affecting
fitness via growth and reproduction (i.e., functional
effect traits) and those responding to alterations in the
environment (i.e., functional response traits) (Hooper
et al., 2002, 2005; Violle et al., 2007). Since many
ecophysiological traits, such as nutrient and light
utilization and grazer resistance, correlate with phy-
toplankton cell size (Litchman & Klausmeier, 2008),
size has been recognized as a master trait. Phyto-
plankton cell size responds to alterations in environ-
mental conditions, like change in water temperature
(Zohary et al., 2020), and also affects ecosystem
functioning (Abonyi et al., 2020). The response of
freshwater phytoplankton size to water temperature
changes seems to be consequent based on both the cell
and colony (filament) size (Zohary et al., 2020).
However, one may consider that cell and colony
(filament) sizes are affected by multiple underlying
mechanisms, and the choose of cell or colony size as
functional trait might be question specific.
The functional group (ecological group) composi-
tion of phytoplankton can be predicted well by the
local environment (Salmaso et al., 2015). However,
the different functional approaches have rarely been
compared in terms of how they affect the community
composition–environment relationship. Kruk et al.
(2011) showed that the morphological group (MBFG)
composition of phytoplankton could be predicted from
the local environment in a more reliable way than
Reynolds’s functional groups (FG), or taxonomic
composition. In a broad-scale phytoplankton dataset
from Fennoscandia, Abonyi et al. (2018a, b) showed
that phytoplankton functional trait categories, as a
community matrix, corresponded with the local envi-
ronment better than Reynolds’s functional groups or
the taxonomic matrix. Along the entire length of the
Atlantic River Loire, Abonyi et al. (2014) showed that
phytoplankton composition based on Reynolds’s FG
classification provided more detailed correspondence
to natural- and human-induced changes in
Hydrobiologia
environmental conditions than based on the morpho-
functional (MFG) and morphological (MBFG)
systems.
The aggregation of taxonomic information into
functional units reduces data complexity that could
come along with reduced ecological information
(Abonyi et al., 2018a, b). Reduced data complexity
can be useful as long as it does not imply serious loss
of ecological information. Information lost can happen
when functional traits are not quantified adequately,
cannot be identified, or when ecologically diverse
taxa, such as benthic diatoms are considered similar
functionally (Wang et al., 2018). Otherwise, the
aggregation of taxonomic to functional data highlights
ecological similarities among taxa (Schippers et al.,
2001) and should lead to better correspondence
between community composition and the environment
(Abonyi et al., 2018a, b).
The functional diversity–ecosystem functioning
relationship
Based on taxonomic data, recent studies support a
positive biodiversity–ecosystem functioning relation-
ship in phytoplankton clearly (Naeem & Li, 1997;
Ptacnik et al., 2008; Striebel et al., 2009). The well-
known paradox of Hutchinson asking how so many
species may coexist in phytoplankton (Hutchinson,
1961) has been reversed to how many species ensure
ecosystem functioning (Ptacnik et al., 2010b). Based
on functional traits, however, almost half of the studies
reported null or negative relationship between func-
tional diversity and ecosystem functioning (Venail,
2017). Recently, Abonyi et al. (2018a, b) argued that
functional diversity based on trait categories (i.e.,
functional trait richness—FTR) and Reynolds’ eco-
logical groups (i.e., functional group richness—FGR)
represented different aspects of community organisa-
tion in phytoplankton. While both functional measures
scaled with taxonomic richness largely, FTR sug-
gested random or uniform occupation of niche space
(Dı́az & Cabido, 2001), while FGR more frequent
niche overlaps (Ehrlich & Ehrlich, 1981), and there-
fore, enhanced functional redundancy (Dı́az &
Cabido, 2001). A key future direction will be to
understand mechanisms responsible for the co-occur-
rence of functional units (‘functional groups’) within
phytoplankton assemblages, and detail phytoplankton
taxa within and among the ecological groups in a trait-
based approach. This will enhance our ability to
disentangle the ecological role of functional redun-
dancy (within groups) and complementarity (among
groups) in affecting ecosystem functioning in the
future.
Phytoplankton diversity using molecular tools
The assessment of phytoplankton diversity in water-
bodies is strongly dependent from the methods used in
the taxonomic identification of species and the quan-
titative estimation of abundances. The adoption of
different methods can strongly influence the number
of taxa identified and the level of detail in the
taxonomic classifications.
Premise: advantages and weaknesses of light
microscopy
Traditionally, phytoplankton microorganisms have
been identified using light microscopy (LM). The
use of this technique was instrumental to lay the
foundation of phytoplankton taxonomy. Many of the
most important and well-known species of nano-
(2–20 lm), micro- (20–200 lm) and macrophyto-
plankton ([ 200 lm) have been identified by several
influential papers and manuals published between the
first half of the 1800 s and first half of 1900 s (e.g.
(Ehrenberg, 1830; de Toni, 1907; Geitler & Pascher,
1925; Guiry & Guiry, 2019). LM is an inexpensive
method providing plenty of information on the mor-
phology and size of phytoplankton morphotypes,
allowing also obtaining, if evaluated, data on abun-
dances and community structure. Conversely, in
addition to being time-consuming, the correct identi-
fication of specimens by LM requires a deep knowl-
edge of algal taxonomy. Further, many taxa have
overlapping morphological features so that the num-
ber of diacritical elements often is not enough to
discriminate with certainty different species (Krienitz
& Bock, 2012; Whitton & Potts, 2012; Wilmotte et al.,
2017). The identification can be further complicated
by the plasticity that characterise a number of
phenotypic characteristics and their dependence from
environmental conditions (Komárek & Komárková,
2003; Morabito et al., 2007; Hodoki et al., 2013;
Soares et al., 2013). The adoption of electron
microscopy for the study of ultra-structural details
has represented an important step in the
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characterization of critical species (e.g. Komárek &
Albertano, 1994) and phyla. For example, in the case
of diatoms, scanning electron microscopy had a huge
impact on diatom taxonomy, making traditional LM
insufficient for the recognition of newly created taxa
(Morales et al., 2001). Since aquatic samples usually
contain many small, rare and cryptic species, a precise
assessment of the current biodiversity is unbearable
with the only use of classic LM (Lee et al., 2014) and
electron microscopy. Nonetheless, despite its limita-
tions, the analysis of phytoplankton by LM still
continues to be the principal approach used in the
monitoring of the ecological quality of waters (Hötzel
& Croome, 1999; Lyche Solheim et al., 2014).
Culture-dependent approaches—classical genetic
characterization of strains
Owing to the above limitations, the identification of
phytoplankton species by LM has been complemented
by the adoption of genetic methods. These methods
are based on the isolation of single strains, their
cultivation under controlled conditions, and their
characterization by polymerase chain reaction (PCR)
and sequencing of specific DNA markers able to
discriminate among genera and species, and some-
times also between different genotypes of a same
species (Wilson et al., 2000; D’Alelio et al., 2013;
Capelli et al., 2017). After sequencing, the DNA
amplicons obtained by PCR can be compared with the
sequences deposited in molecular databases, e.g. those
included in the International Nucleotide Sequence
Database Collaboration (INSDC: DDBJ, ENA, Gen-
Bank) using dedicated tools, such as BLAST queries
(Johnson et al., 2008). Further, the new sequences can
be analysed, together with different homologous
sequences, to better characterize the phylogenetic
position and taxonomy of the analysed taxa in specific
clades (Rajaniemi et al., 2005; Krienitz & Bock, 2012;
Komárek et al., 2014). The phylogenetic analyses
provide essential information also for evaluating the
geographical distribution of species (Dyble et al.,
2002; Capelli et al., 2017) and their colonization
patterns (Gugger et al., 2005), to infer physiological
traits (Bruggeman, 2011), and to evaluate relation-
ships between phylogeny and sensitivity to anthro-
pogenic stressors in freshwater phytoplankton (Larras
et al., 2014). The selection of primers and markers, and
their specificity to target precise algal groups is an
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Hydrobiologia
essential step, which strictly depends on the objectives
of investigations and availability of designated
databases. For example, though 16S and 18S rRNA
genes are the most represented in the INSDC
databases, dedicated archives have been curated for
the blast and/or phylogenetic analyses of cyanobacte-
ria (e.g. Ribosomal Database Project; Quast et al.,
2013; Cole et al., 2014) and eukaryotes (e.g. Quast
et al., 2013; Rimet et al., 2019). Further, an increase in
the sensitivity of the taxonomic identification based on
DNA markers can be obtained through the concurrent
analysis of multiple genes using Multilocus Sequence
Typing (MLST) and Multilocus Sequence Analysis
(MLSA) (see Wilmotte et al., 2017, for details).
A potential issue with the single use of only
microscopy or genetic methods is due to the existence
of genetically almost identical different morphotypes
and to the development of uncommon morphological
characteristics in strains cultivated and maintained in
controlled culture conditions. To solve these prob-
lems, a polyphasic approach has been proposed, which
makes use of a set of complementary methods, based
besides genetics, on the analysis of phenotypic traits,
physiology, ecology, metabolomics and other charac-
ters relevant for the identification of species of
different phyla (Vandamme et al., 1996; Komárek,
2016; Salmaso et al., 2017; Wilmotte et al., 2017).
Considering the existence of different genotypes
within a single species (D’Alelio et al., 2011; Yarza
et al., 2014), the genetic characterizations of phyto-
plankters have to be performed at the level of single
strain. Excluding single cell sequencing analyses (see
below), the methods have to be therefore applied to
isolated and cultivated strains. This represents a huge
limitation for the assessment of biodiversity, because
the analyses are necessarily circumscribed only to the
cultivable organisms. The rarest and the smaller ones
are equally lost. Further, the genetic and/or the
polyphasic approaches are time-consuming, allowing
to process only one species at a time. To solve this
limitation, a set of culture-independent approaches to
assess biodiversity in environmental samples have
been developed since the 1980s.
Culture independent approaches—traditional
methods
A consistent number of molecular typing methods
based on gel electrophoresis and a variety of other
Hydrobiologia
approaches (e.g. quantitative PCR-qPCR) have been
applied since the 1980 s and 1990 s in the analysis of
microbial DNA, including ‘‘phytoplankton’’ (for a
review, see Wilmotte et al., 2017). These approaches
are tuned to target common regions of the whole
genomic DNA extracted from water samples or other
substrata, providing information on the existence of
specific taxonomic and toxins encoding genes (Campo
et al., 2013; Capelli et al., 2018), and the taxonomic
composition of the algal community without the need
to isolate and cultivate individual strains. In this latter
group of methods, probably one of the most used in
phytoplankton ecology is the denaturing gradient gel
electrophoresis (DGGE; (Strathdee & Free, 2013).
Taking advantage of the differences in melting
behaviours of double-stranded DNA in a polyacry-
lamide gel with a linear gradient of denaturants,
DGGE allows the differential separation of DNA
fragments of the same length and different nucleotide
sequences (Jasser et al., 2017). This technique is able
to discriminate differences in single-nucleotide poly-
morphisms without the need for DNA sequencing,
providing information at level of species and geno-
types. For example, analysing samples from eight
lakes of different trophic status, Li et al. (2009)
identified complex community fingerprints in both
planktic eukaryotes (up to 52 18S rDNA bands) and
prokaryotes (up to 59 16S rDNA bands). If coupled
with the analyses of excised DNA bands (Callieri
et al., 2007), or with markers composed of cyanobac-
terial clone libraries (Tijdens et al., 2008), DGGE can
provide powerful indications on the diversity and
taxonomic composition of phytoplankton. More
recent examples of the application of this technique
to phytoplankton and eukaryotic plankton are given in
Dong et al. (2016), Batista & Giani (2019). A recent
comparison of DGGE with other fingerprint methods
(Terminal restriction fragment length polymorphism,
TRFLP) was contributed by Zhang et al. (2018).
A second method that has been used in the
characterization of phytoplankton from microbial
DNA is fluorescence in situ hybridization (FISH),
and catalysed reporter deposition (CARD)-FISH
(Kubota, 2013). In freshwater investigations, this
technique has been used especially in the evaluation
of prokaryotic communities (Ramm et al., 2012). A
third method deserving mention is cloning and
sequencing (Kong et al., 2017).
In principle, compared to LM and traditional
genetic methods, these techniques can provide an
extended view of freshwater biodiversity. Neverthe-
less, they suffer from several limitations, due to the
time, costs and expertise required for the analysis, and
the incomplete characterization of biodiversity due to
manifest restrictions in the methods (e.g. finite reso-
lution of gel bands in DGGE and number and
sensitivity of markers to be used in CARD-FISH).
Part of these limits have been solved with the adoption
of new generation methods based on the analysis of
environmental and microbial DNA.
Culture independent approaches—metagenomics
The more modern methods boost the sequencing
approach over the traditional constraints, allowing
obtaining, without gel-based methods or cloning,
hundreds of thousands of DNA sequences from
environmental samples using high throughput
sequencing (HTS). Under the umbrella of metage-
nomics, we can include a broad number of specialized
techniques focused on the study of uncultured
microorganisms (microbes, protists) as well as plants
and animals via the tools of modern genomic analysis
(Chen & Pachter, 2005; Fujii et al., 2019). The
methods based on HTS analysis of microbial DNA can
be classified under two broad categories, i.e. studies
performing massive PCR amplification of certain
genes of taxonomic or functional interest, e.g. 16S
and 18S rRNA (marker gene amplification metage-
nomics), and the sequence-based analysis of the whole
microbial genomes extracted from environmental
samples (full shotgun metagenomics) (Handelsman,
2009; Xia et al., 2011). While full shotgun metage-
nomics techniques were used in the first global
investigations of marine biodiversity (Venter et al.,
2004; Rusch et al., 2007; Bork et al., 2015), the use of
marker gene amplification metagenomics in the study
of freshwater phytoplankton has shown an impressive
increase in the last decade. The reasons are still due to
the minor costs (a few tens of euros per sample) and
the simpler bioinformatic tractability of sequences of
specific genes compared to full shotgun
metagenomics.
The large progress and knowledge obtained in the
study of microbial communities (Bacteria and
Archaea) based on the analysis of the 16S rDNA
marker in the more disparate terrestrial, aquatic and
123

host-organisms’ habitats (e.g. gut microbial commu-
nities) had a strong influence in directing the type of
investigations undertaken in freshwater environments.
At present, the majority of the investigations in
freshwater habitats are focused on the identification
of microbial (including cyanobacteria) communities,
with a minority of studies focused on the photosyn-
thetic and mixotrophic protists (phytoplankton) eval-
uated through deep sequencing of the 18S rDNA
marker (e.g. (Mäki et al., 2017; Li & Morgan-Kiss,
2019; Salmaso et al., 2020).
The results obtained from the applications of HTS
to freshwater samples are impressive and are unveiling
a degree of diversity in biological communities
previously unimaginable, including a significant pres-
ence of the new group of non-photosynthetic
cyanobacteria (Shih et al., 2013, 2017; Salmaso
et al., 2018; Monchamp et al., 2019; Salmaso, 2019).
Nonetheless, the application of these techniques is not
free from difficulties, due to (among the others) the
semiquantitative nature of data, the short DNA reads
obtained by the most common HTS techniques, the
variability in the copy number per cell of the most
common taxonomic markers used (i.e. 16S and 18S
rDNA), the incompleteness of genetic databases,
which are still fed by information obtained by the
isolation and cultivation approaches (Gołe˛biewski &
Tretyn, 2020; Salmaso et al., 2020). Despite these
constraints, the use of HTS techniques in the study of
phytoplankton, which is just at the beginning, is
contributing to revolutionize the approach we are
using in the assessment of aquatic biodiversity in
freshwater environments, opening the way to a next
generation of investigations in phytoplankton ecology
and a new improved understanding of plankton
ecology.
Conclusions
In this study, we reviewed various aspects of phyto-
plankton diversity, including definitions and mea-
sures, mechanisms maintaining diversity, its
dependence on productivity, habitat size and temper-
ature, functional diversity in the context of ecosystem
functioning, and molecular diversity.
Phytoplankton diversity cannot be explained with-
out the understanding of mechanisms that shape
assemblages. We highlighted how Vellend’s
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framework on community assembly (speciation,
selection, drift, dispersal) could be applied to phyto-
plankton assemblages. Competition theories and non-
equilibrium approaches fitted also well into this
framework.
The available literature on phytoplankton species–
area relationship contains information on isolated
habitats. These studies argue that richness depends on
habitat size. However, findings on eutrophic shallow
water bodies suggest that habitat diversity can modify
the monotonous increasing tendencies and hump-
shaped relationship might occur. The literature on
lake’s phytoplankton productivity–diversity relation-
ship supports trends reported for terrestrial ecosys-
tems, i.e. a humped shape relationship at local scale if
a sufficiently large productivity range is considered.
However, the shapes of the curves depend also on the
types of the water bodies. In rivers, both monotonic
increasing (rhithral rivers) and decreasing (potamal
rivers) trends could be observed.
The aggregation of phytoplankton taxonomic data
based on functional information reduces data com-
plexity largely. The reduced biological information
could come along with ecological information loss,
e.g. when traits cannot be quantified adequately, or,
when ecologically diverse taxa are considered similar
functionally. Since pelagic phytoplankton is relatively
similar functionally, the aggregation of taxonomic into
functional data can highlight ecological similarities
among taxa in a meaningful way. Accordingly,
functional composition and diversity may help better
relate phytoplankton communities to their environ-
ment and predict the effects of community changes on
ecosystem functioning.
The adoption of a new generation of techniques
based on the massive sequencing of selected DNA
markers and planktonic genomes is beginning to
change our present perception of phytoplankton
diversity. Moreover, being ‘‘all-inclusive’’ techniques,
HTS are contributing to change also the traditional
concept of ‘‘phytoplankton’’, providing a whole pic-
ture not only of the traditional phytoplankton groups,
but of the whole microbial (including cyanobacteria)
and protist (including phytoplankton) communities.
The new molecular tools not only help species
identification and unravel cryptic diversity, but
provide information on the genetic variability of
species that determine their metabolic range and
unique physiological properties. These, basically
Hydrobiologia
influence speciation and species performances in
terms of biotic interactions or colonisation success,
and thus affect species assembly.
Outlook
Overexploitation of ecosystems and habitat destruc-
tions coupled with global warming resulted in huge
species loss on Earth. The rate of diversity loss is so
high that scientists agree that the Earth’s biota entered
the sixth mass extinction (Ceballos et al., 2015). While
population shrinkage or extinction of a macroscopic
animal receive large media interest (writing this
sentence we have the news that the Chinese paddle-
fish/Psephurus gladius/declared extinct), extinction
rate of poorly known taxa can be much higher
(Régnier et al., 2015). Phytoplankton, invertebrates
and microscopic organisms belongs to groups where
extinctions do occur, but the rate of extinctions cannot
be assessed. Worldwide, thousands of phytoplankton
samples are investigated every day, mostly for water
quality monitoring purposes. However, assessment
methods focus on the identification of the dominant
and subdominant taxa, because these determine
mostly the values of quality metrics. Since species
richness or abundance-based diversity metrics are not
considered as good quality indicators (Carvallho et al.,
2013), investigators are not forced to reveal the overall
species richness of the samples. To give an accurate
prediction for the species richness of a water body, an
extensive sampling strategy and the use of species
estimators would be required. Nevertheless, high local
species richness does not necessarily mean good
ecosystem health and high nature conservation value;
e.g. if weak selection couples with high number of new
invaders. Small water bodies with low local alpha
diversity but with unique microflora can have high
conservation value (Bolgovics et al., 2019). Preserva-
tion of large phytoplankton species diversity at the
landscape or higher geographic level needs to main-
tain high beta diversity by the protection of unique
habitats (Noss, 1983). Because of the multiple human
impacts and global warming, small water bodies
belong to the most endangered habitats whose protec-
tion is of paramount importance.
Our understanding about phytoplankton diversity
has progressed in the recent decades. These were
mainly motivated by elucidating mechanisms that
drive diversity, and by the emergence of new
approaches for analysing relationships between diver-
sity and ecosystem functioning.
Increasing human pressure and global warming-
induced latitudinal shifts in climate zones, resulting in
hydrological regime shifts with serious implications
for aquatic ecosystems including phytoplankton.
These timely challenges will also affect near future
trends in phytoplankton studies. The sound theoretical
principles, together with the new molecular and
statistical tools open new perspectives in diversity
research, which, may let us hope that the Golden Age
of studying phytoplankton diversity lies before us and
not behind.
Dedication
Each study in this special issue of Hydrobiologia is
dedicated to the memory of the late Colin S. Reynolds,
who made an outstanding contribution to aquatic
science, and considered one of the most prominent
phytoplankton ecologists of the last three decades. His
encyclopedic work, The ecology of phytoplankton
(2006) considered by many as the Bible for lake
phytoplankton ecology, and serves still as a reference
for many recent works. His oeuvre covers a wide range
of topics within aquatic ecology, including community
assembly, functional approaches, modelling of bio-
mass production, resilience and health of aquatic
ecosystems. Reynolds’s contribution to our under-
standing of diversity maintenance mechanisms is still
relevant and served as a basis for shaping our
manuscript.
Acknowledgements Open access funding provided by ELKH
Centre for Ecological Research. BG was supported by the
GINOP-2.3.2-15-2016-00019 project and by the NKFIH OTKA
K-132150 Grant. NS was supported by the co-financing of the
European Regional Development Fund through the Interreg
Alpine Space programme, project Eco-AlpsWater (Innovative
Ecological Assessment and Water Management Strategy for the
Protection of Ecosystem Services in Alpine Lakes and Rivers -
https://www.alpine-space.eu/projects/eco-alpswater). AA was
supported by the National Research, Development and Inno-
vation Office, Hungary (NKFIH, PD 124681).
Open Access This article is licensed under a Creative Com-
mons Attribution 4.0 International License, which permits use,
sharing, adaptation, distribution and reproduction in any med-
ium or format, as long as you give appropriate credit to the
original author(s) and the source, provide a link to the Creative
123

Commons licence, and indicate if changes were made. The
images or other third party material in this article are included in
the article’s Creative Commons licence, unless indicated
otherwise in a credit line to the material. If material is not
included in the article’s Creative Commons licence and your
intended use is not permitted by statutory regulation or exceeds
the permitted use, you will need to obtain permission directly
from the copyright holder. To view a copy of this licence, visit
http://creativecommons.org/licenses/by/4.0/.
Authors contributions BG wrote ‘Introduction’, ‘Mechanisms
affecting diversity’, ‘Diversity measures’, Changes of diversity
along environmental scales, ‘Conclusions’ and ‘Outlook’ with
substantial contribution from RP. AA, RP wrote ‘The functional
diversity–ecosystem functioning relationship in phytoplankton’,
NS wrote ‘Phytoplankton diversity using molecular tools’
chapters.
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